Buprofezin Susceptibility Survey, Resistance Selection And

Pest Management Science Pest Manag Sci 64:1050–1056 (2008)

Buprofezin susceptibility survey, resistance selection and preliminary determination of the resistance mechanism in Nilaparvata lugens (Homoptera: Delphacidae) Yanhua Wang,1,2 Congfen Gao,1 Zhiping Xu,1 Yu Cheng Zhu,3∗ Jiushuang Zhang,1 Wenhong Li,1 Dejiang Dai,1 Youwei Lin,1 Weijun Zhou,1 and Jinliang Shen1∗ 1Key Laboratory of Monitoring and Management of Plant Disease and Insects, Ministry of Agriculture/Department of Pesticide Science, College of Plant Protection, Nanjing Agricultural University, Nanjing 210095, China 2Institute of Quality and Standard for Agro-products, Zhejiang Academy of Agricultural Sciences, Hangzhou 310021, China, 3Jamie Whitten Delta States Research Center, ARS-USDA, Stoneville, MS 38776, USA Abstract

BACKGROUND: Buprofezin has been used for many years to control Nilaparvata lugens (Stal).˚ Assessment of susceptibility change in the insect is essential for maintaining control efﬁciency and resistance management.

RESULTS: Eleven-year surveys showed that most field populations were susceptible before 2004. However, substantially higher levels of resistance (up to 28-fold) were found in most of the rice fields in China after 2004. A field population was collected and periodically selected for buprofezin resistance in the laboratory. After 65 generations (56 were selected), the colony successfully obtained 3599-fold resistance to buprofezin. Synergism tests showed that O,O-diethyl-O-phenyl phosphorothioate (SV1), piperonyl butoxide (PBO) and diethyl maleate (DEM) increased buprofezin toxicity in the resistant strain by only 1.5–1.6 fold, suggesting that esterases, P450- monooxygenases and glutathione S-transferases had no substantial effect on buprofezin resistance development.

CONCLUSION: The results from this study indicate that N. lugens has the potential to develop high resistance to buprofezin. A resistance management program with rotation of buprofezin and other pesticides may efﬁciently delay or slow down resistance development in the insect. Further investigation is also necessary to understand the resistance mechanisms in N. lugens.  2008 Society of Chemical Industry

Keywords: Nilaparvata lugens; buprofezin; susceptibilities; resistance mechanism

1 INTRODUCTION especially effective against Homoptera pests, such as The brown planthopper, Nilaparvata lugens (Stal),˚ the planthopper, with very low risks to the environ- is a major rice pest in China and one of the most ment and humans.9–11 Its mode of action is not fully damaging agricultural insect pests in many parts of understood, although the primary effect is to interfere Asia.1,2 Managing the pest with insecticides remains with chitin deposition during molting and to cause the single most frequently used method, in the absence nymphal death during ecdysis.10 In addition, reduced of other effective methods.3 Therefore, resistance to fecundity and egg hatching have been observed after various synthetic insecticides has been observed in adult females were treated.12,13 Although buprofezin many locations.4–6 Nilapavata lugens is a migratory lacks an acute insecticidal effect, it offers the advantage insect and is able to travel long distances between of longer residual activity against N. lugens nymphs the southern and the northern parts of China.7 This than conventional insecticides. Therefore, buprofezin migration may slow down resistance development was thought by many researchers to be a unique through dilution, or speed up resistance development insecticide for controlling the planthopper, and the in destination areas, depending on the resistance levels registration of buprofezin in the 1980s signaled an in the original areas and the nature of resistance to important landmark in the chemical control of the different insecticides.8 pest in China.14 Buprofezin remained an important Buprofezin, a chitin synthesis inhibitor developed chemical for planthopper control until the early 1990s by Nihon-Nohyaku, is a thiadiazine insecticide that is when imidacloprid was introduced for controlling the

∗ Correspondence to: Yu Cheng Zhu, USDA-ARS-JWDSRC, PO Box 346, Stoneville, MS 38776, USA E-mail: [email protected] Jinliang Shen, Key Laboratory of Monitoring and Management of Plant Disease and Insects, Ministry of Agriculture, Nanjing Agricultural University, Nanjing 210095, China E-mail: [email protected]; (Received 29 October 2007; revised version received 23 February 2008; accepted 24 February 2008) Published online 27 May 2008; DOI: 10.1002/ps.1606

 2008 Society of Chemical Industry. Pest Manag Sci 1526–498X/2008/$30.00 Susceptibility of Nilaparvata lugens to buprofezin insect.15 In recent years, buprofezin has again been to indicate the generations since the first selection with recommended as one of the main alternatives for buprofezin. replacing methamidophos. Resistance development to buprofezin was first detected in whitefly populations in 2.2 Insecticide greenhouses in the Netherlands,16 and subsequently A commercial buprofezin 250 g kg−1 WP was supplied in northern Europe, Spain and Israel.17,18 However, by Changlong Chemical Industrial Group Co. Ltd because of buprofezin’s unique nature, especially its (Changzhou, Jiangsu, China) and was used for novel mode of action, resistance development in field testing the susceptibility of N. lugens during the populations appears to be very slow, and the resistance years from 1996 to 2006. SV1 (O,O-diethyl-O-phenyl mechanisms are not well understood. phosphorothioate, 500 g L−1 EC) was from Changlong Because of its long application history and Chemical Industrial Group Co. Ltd (Hangzhou, widespread adoption, decreased susceptibility to Zhejiang, China). Piperonyl butoxide (PBO, 800 g L−1 buprofezin in N. lugens has become a major con- EC) and diethyl maleate (DEM, reagent grade) were cern in rice-growing regions in China. To provide a from Acros Organics of America (Morris Plains, NJ). foundation for area-wide resistance management of N. lugens, the authors initiated a study to investi- 2.3 Bioassay gate regional and temporal changes in susceptibility The rice-stem dipping method19– 21 was adopted in to buprofezin in rice production areas. In addition, a this study. Rice stems, including roots, were pulled out buprofezin-resistant strain of N. lugens was developed and washed thoroughly. The basal 10 cm long stems by laboratory selection for evaluation of the risk of were cut and air dried to remove excess water. Three resistance development and preliminary determination rice stems were grouped and dipped into appropriate of the resistance mechanisms in N. lugens. insecticide test solutions for 30 s. Three replicates were used per dose, and 5–6 doses plus water only as the control were used for each chemical. After the 2 MATERIALS AND METHODS rice stems had been air dried for approximately 1 h, 2.1 Insects moistened cotton was used to wrap the basal end of the The susceptible strain of N. lugens was originally rice roots. Treated rice stems were then placed into a collected in 1993 from a rice nursery located at the 500 mL plastic cup. Twenty third-instar nymphs were Plant Protection Station of Jiangpu County (Jiangsu, introduced into each plastic cup using a suction device. China). The insects were reared on hybrid rice The treated insects were maintained at 27 ± 1 ◦Cand (Shanyou 63), and an isoline was established from 16:8 h light:dark photoperiod. Mortality was recorded a single-pair mating method in the laboratory. after 120 h. The nymphs were considered dead if To examine buprofezin resistance in different rice- they were unable to show coordinated movement after growing areas, a total of 45 samples were collected gentle prodding with a fine bristle. from 27 locations in eight different provinces or autonomous regions from 1996 to 2006. Selection 2.4 Resistance selection of these sites was based on their importance for Rice stems were treated with buprofezin using the rice production and their history and intensity of dipping method and were transferred into a cage insecticide applications. In addition, these locations (57 × 57 × 92 cm). Approximately 1000 third-instar were also allocated and considered for further nymphs of N. lugens were introduced into the resistance monitoring and analysis. Approximately cage and subsequently maintained at 27 ± 1 ◦Cand 800 adults, 500–600 nymphs or sufficient egg masses 16:8 h light:dark photoperiod for 5 days. Survivors were collected at each site and transported to the were transferred to another cage containing fresh greenhouse on the campus of Nanjing Agricultural rice seedlings. Pre-trials were conducted to obtain University. The insects were reared on insecticide- an optimal insecticide concentration for resistance free hybrid rice (Shanyou 63) before bioassays were selection. The mortality was controlled to a range performed. The same rice variety at tillering to booting between 40 and 70% to ensure sufficient survivors stage was used for maintaining insect colonies and to develop and reproduce enough progenies for the subsequent bioassays. Field-collected insects were insecticide selection of the subsequent generation. The mass mated. The third-instar nymphs of F1 progenies treatment concentration was approximately the same were used for bioassays. All treated insects were as the LC50 obtained for each generation. maintained at a temperature of 27 ± 1 ◦C and a 16:8 h light:dark photoperiod. 2.5 Test for synergism To investigate the synergistic effect of major metabolic 2.1.1 Anqing population (AQ) enzyme inhibitors on the efficacy of buprofezin, SV1, Nilparvata lugens adults of an immigrated generation PBO and DEM were individually added to each were collected in 1996 from a rice field of Anqing serial concentration of buprofezin. Pre-trial tests were Academy of Agricultural Science (Anhui, China). The conducted to determine the highest concentration for insects were reared for ten generations and then used each synergist (SV1 5 mg L−1;PBO20mgL−1;DEM for resistance selection with buprofezin. Gn was used 500 mg L−1), with no obvious detrimental effects on

Pest Manag Sci 64:1050–1056 (2008) 1051 DOI: 10.1002/ps YWanget al. the third-instar nymphs of either population of N. respectively) in 1996. However, a medium resistance lugens. Other experimental procedures were the same level to buprofezin (RR = 28.1) was found in the Nan- as described above. To assess the degree of synergism, jing population in 2005 (Table 2), where the insects the synergistic ratio (SR) was calculated by dividing were repeatedly assayed from 1996 to 2004 and their the LC50 value of buprofezin alone by the LC50 value resistance ratios were no more than 5-fold. The other of buprofezin plus synergist. 14 populations from Jiangsu, Zhejiang, Anhui and Jiangxi provinces also developed low resistance levels 2.6 Data analysis to the insecticide (RR = 5.9–9.7) in 2005. Further The POLO program was used for probit analysis resistance surveys in 2006 (Table 2) indicated that of dose–response data,22 unless otherwise stated. twelve field populations of N. lugens from Guangxi, Mortality was corrected using Abbott’s formula for Jiangxi, Jiangsu, Hubei, Zhejiang, Anhui and Fujian each probit analysis.23 The resistance ratio (RR) was provinces developed minor to low-level resistance to = calculated by dividing the LC50 of a field population buprofezin (RR 2.5–9.4), which did not increase by the LC50 of the susceptible strain. Significant level substantially but maintained median levels similar to of mean separation (P < 0.05) was based on non- those during the same period in 2005. overlap between the 95% confidence limits (CL) of two LC50 values. Resistance levels were classified on 3.2 Buprofezin resistance selection the basis of the standard described by Shen and Wu24 For the selection tests, the experiments lasted 65 gen- as susceptible (RR < 3-fold), minor resistance (RR = erations. Fifty-six generations were treated with bupro- 3–5-fold), low resistance level (RR = 5–10-fold), fezin, and the other nine generations (F6-F9, F15-F17 medium resistance level (RR = 10–40-fold), high and F19-F20) were not treated with the insecticide. resistance level (RR = 40–160-fold) and extremely Results of the buprofezin resistance selection (Fig. 1) high resistance level (RR > 160-fold). showed that resistance ratios varied substantially over the 65-generation selection period. In the first 25 generations, selection with buprofezin did not reveal a 3RESULTS distinct increase in resistance ratios, which only fluc- 3.1 Dose response and resistance level in field tuated between 1.5 and 3.9. From generation 26 to populations generation 32, the resistance ratios quickly increased to The LC50 value of buprofezin in the susceptible strain 1037.3-fold. After that, the resistance ratios continued was 0.268 (0.21–0.32) mg AI L−1 (Tables 1 and 2). A to increase at a relatively slow pace until generation total of 45 field samples collected from eight provinces 53 (G53), which obtained a 1658.2-fold resistance were examined from 1996 to 2006 for their susceptibil- ratio. A rapid increase in resistance ratios appeared ity to buprofezin. The results showed that most of the again in the subsequent 12 generations. Generation N. lugens populations from Jiangsu (Nanjing, Yizheng 65 (G65) showed the highest resistance to bupro- and Nantong), Anhui (Anqing) and Guangxi (Guilin) fezin (RR = 3598.9-fold) in the total 65 generations remained susceptible (RR < 3) to buprofezin from tested. It was likely that the resistance level of N. 1996 to 2004, except for the Anqing and Nanjing pop- lugens to buprofezin would have increased further if ulations with minor resistance (RR = 3.3- and 3.5-fold the selection had continued.

Table 1. Dose response and resistance ratio (RR) to buprofezin in ﬁeld populations of Nilaparvata lugens collected from 1996 to 2004

Test populations Dose response

−1 Years Provinces Locations Slope (±SE) LC50 (mg AI L ) (95%CI) RR Susceptible strain 2.89 (±0.23) 0.268 (0.21–0.32) 1.0 1996 Anhui Anqing 4.05 (±0.48) 0.90 (0.81–0.96) 3.3 Guangxi Guilin 2.77 (0.19) 0.47 (0.36–0.56) 1.7 Guangxi Nanning 4.95 (±0.37) 0.77 (0.72–0.83) 2.9 Jiangsu Nanjing 1.66 (±0.14) 0.95 (0.78–1.30) 3.5 1997 Anhui Anqing 3.30 (±0.28) 0.67 (0.61–0.73) 2.5 Guangxi Guilin 2.44 (±0.19) 0.53 (0.44–0.61) 2.0 Guangxi Nanning 2.71 (±0.23) 0.81 (0.77–0.86) 3.0 Jiangsu Nanjing 4.78 (±0.51) 0.59 (0.41–0.62) 2.2 1998 Guangxi Nanning 2.71 (±0.22) 0.38 (0.32–0.44) 1.4 Jiangsu Yizheng 4.73 (±0.57) 0.43 (0.38–0.47) 1.6 1999 Guangxi Nanning 2.38 (±0.23) 0.44 (0.39–0.49) 1.6 Jiangsu Nantong 2.04 (±0.17) 0.38 (0.32–0.42) 1.4 2001 Jiangsu Nanjing 1.92 (±0.14) 0.39 (0.32–0.47) 1.5 2002 Guangxi Nanning 2.29 (±0.25) 0.67 (0.58–0.76) 2.5 2003 Jiangsu Nanjing 2.09 (±0.18) 0.48 (0.40–0.58) 1.8 2004 Jiangsu Nanjing 2.60 (±0.23) 0.61 (0.52–0.72) 2.3

1052 Pest Manag Sci 64:1050–1056 (2008) DOI: 10.1002/ps Susceptibility of Nilaparvata lugens to buprofezin

Table 2. Dose response and resistance ratio (RR) to buprofezin in ﬁeld populations of Nilaparvata lugens collected in 2005 and 2006

Test populations Dose response

−1 Year Month Provinces Locations Slope (± SE) LC50 (mg AI L ) (95% CI) RR 2005 August Guangxi Guilin 2.15 (±0.21) 2.18 (1.76–2.60) 8.1 2005 August Guangxi Nanning 2.07 (±0.20) 1.59 (0.84–2.60) 5.9 2005 August Hunan Changde 1.87 (±0.24) 2.60 (1.51–3.60) 9.7 2005 August Jiangsu Nanjing 1.64 (±0.18) 7.54 (5.86–9.63) 28.1 2005 September Anhui Caohu 1.47 (±0.12) 1.76 (1.42–2.01) 6.6 2005 September Jiangsu Gaochun 1.56 (±0.16) 2.01 (1.59–2.60) 7.5 2005 September Jiangsu Suzhou 1.46 (±0.13) 1.68 (1.34–2.01) 6.3 2005 September Jiangsu Wuxi 1.62 (±0.17) 2.09 (1.51–2.93) 7.8 2005 September Zhejiang Haiyan 1.46 (±0.16) 1.59 (1.26–2.01) 5.9 2005 September Zhejiang Jiaxing 1.62 (±0.18) 2.09 (1.68–2.68) 7.8 2005 September Zhejiang Shaoxing 1.99 (±0.19) 2.01 (1.68–2.43) 7.5 2005 September Zhejiang Tongxiang 1.31 (±0.16) 2.43 (1.84–3.18) 9.1 2005 September Zhejiang Yuyao 1.84 (±0.22) 1.68 (1.34–2.18) 6.3 2005 October Anhui Hexian 1.34 (±0.16) 1.93 (1.42–2.51) 7.2 2005 October Jiangxi Nanchang 1.30 (±0.20) 1.68 (1.26–2.26) 6.3 2005 October Jiangxi Xinjian 1.74 (±0.19) 1.59 (1.26–2.01) 5.9 2006 June Guangxi Nanning 2.75 (±0.25) 2.51 (2.18–2.93) 9.4 2006 July Jiangxi Shanggao 2.57 (±0.28) 1.09 (0.92–1.34) 4.1 2006 August Hubei Xiaogan 2.57 (±0.28) 1.09 (0.84–1.34) 4.1 2006 August Jiangsu Nanjing 2.38 (±0.25) 1.51 (1.26–1.84) 5.6 2006 August Zhejiang Jinhua 2.07 (±0.21) 0.67 (0.50–0.84) 2.5 2006 September Anhui Hexian 2.04 (±0.21) 1.51 (1.27–1.84) 5.6 2006 September Anhui Ningguo 2.09 (±0.21) 1.51 (1.27–1.68) 5.6 2006 September Anhui Qianshan 2.33 (±0.26) 2.26 (1.84–2.68) 8.4 2006 September Fujian Fuqing 2.07 (±0.20) 1.17 (0.84–1.59) 4.4 2006 September Jiangsu Tongzhou 2.73 (±0.28) 1.59 (1.34–1.93) 5.9 2006 September Zhejiang Haiyan 2.30 (±0.25) 1.59 (1.34–1.93) 5.9 2006 October Jiangsu Dongtai 2.04 (±0.20) 1.68 (1.42–1.93) 6.3

Figure 1. Change in resistance ratios to buprofezin in N. lugens under different selection pressures. Among the 44 generations treated with buprofezin, 22 generations were measured for LC50 and RR (ž), and 22 generations were not measured for RR ( ). Nine generations were not treated with buprofezin (×). The o and × points are for connection only and have no RR value. °

3.3 Effect of synergists on buprofezin these metabolic enzymes can enhance insecticide tox- resistance icity. Synergistic effects of SV1, PBO and DEM on SV1, PBO and DEM inhibit esterases and P450 buprofezin were tested on the susceptible and G65 monooxygenases, P450 monooxygenases and glu- resistant strains of N. lugens. The results (Table 3) tathione S-transferases respectively. The inhibition of indicate that synergistic ratios of SV1, PBO and DEM

Pest Manag Sci 64:1050–1056 (2008) 1053 DOI: 10.1002/ps YWanget al.

Table 3. Synergistic effects of SV1, PBO and DEM on buprofezin in susceptible (S) and buprofezin-selected G65 strains of Nilaparvata lugens

−1 a Strain Treatment Slope LC50 (mg AI L ) (95% CI) Synergism ratio Relative synergism ratio S Buprofezin 2.3475 0.268 (0.21–0.32) 1 – SBuprofezin+ SV1 2.3182 0.14 (0.11–0.17) 1.9 – SBuprofezin+ PBO 2.8187 0.17 (0.13–0.20) 1.6 – SBuprofezin+ DEM 2.7732 0.19 (0.15–0.23) 1.4 – G65 Buprofezin 1.9310 964.50 (755.77–1151.65) 1 – G65 Buprofezin + SV1 1.5811 321.50 (251.92–383.88) 3.0 1.6 G65 Buprofezin + PBO 1.8748 401.88 (314.90–479.85) 2.4 1.5 G65 Buprofezin + DEM 1.9025 459.29 (359.89–548.40) 2.1 1.5 a Relative synergism ratio = synergism ratio of resistant strain/synergism ratio of susceptible strain. were 1.9, 1.6 and 1.4-fold in the S strain, and 3.0, 2.4 each year when the population density increased to a and 2.1-fold in the G65 resistant strain respectively. serious level. In spite of that, buprofezin was still a The relative synergism ratios (synergism ratio in the less prevalently used insecticide than imidacloprid and G65 resistant strain divided by the synergism ratio other insecticides for controlling N. lugens after the in the susceptible strain) were 1.6-, 1.5- and 1.5-fold 1990s.28 Secondly, N. lugens is a typical long-distance for SV1, PBO and DEM respectively. These results migratory pest, and the inheritance of resistance to indicate that esterases, P450-monooyxgenases and buprofezin was incompletely recessive.34 After migra- glutathione S-transferases had no substantial effect tion, heterozygous (susceptible) offspring are pro- on buprofezin resistance development in N. lugens. duced at destination sites, considering the emigrating and resident populations to have different genotypes (susceptibilities) to the insecticide. Therefore, migra- 4 DISCUSSION tion plays a substantial role in delaying resistance Before the mid-1990s, buprofezin, along with car- development through diluting high-level resistance.35 bamates and organophosphates, played an important So, infrequent use of buprofezin and migration might role in N. lugens control.2,4,25 Owing to its unique have effectively kept the resistance development under action on the ecdysis of the nymphal stage,26 bupro- control until 2004, when only a minor level of resis- fezin became more valuable in chemical control of the tance was detected in many rice-growing areas. The planthoppers. However, imidacloprid, first introduced resistance increase since 2005 may be associated with in the early 1990s in China, quickly became a dom- intensified application of buprofezin after the insect inant insecticide owing to its systemic and relatively became highly resistant to imidacloprid, the dominant fast action against the insect,27 whichresultedinan insecticide for planthopper control. apparent decrease in buprofezin applications.28 How- Owing to the incompletely recessive nature of ever, the development of a high to extremely high level the resistance to buprofezin, the authors’ eleven- of resistance to imidacloprid in N. lugens was found year surveys indicated that the rate of resistance in many rice fields in 2005 (data not shown). There- development to buprofezin was much slower than fore, buprofezin was recommended again as the main resistance development to imidacloprid in N. lugens. insecticide for planthopper control. Current resistance development to buprofezin might Nilaparvata lugens remained susceptible to minor be at an early stage or in a slow increase phase. resistance levels to buprofezin from 1996 to 2004, Whether or not a rapid increase will happen sooner but low to medium resistance levels were found in or later depends on selection pressure, e.g. application the majority of rice fields in 2005. Widespread and intensity in the field. long-term usage of buprofezin was probably the main Rotating buprofezin with other insecticides (such reason for the development of a medium resistance as chlorpyrifos, fipronil, isoprocarb, dichlorovos, level to the insecticide in N. lugens. Similar situations pymetrozine and many others) with different modes of resistance increase due to extensive and intensive of action can reduce selection pressure and delay applications have also been observed in many other or slow down resistance development in N. lugens. insects, such as imidacloprid resistance development The present laboratory selection data (Fig. 1) showed in Leptinotarsa decemlineata (Say) and Bemisia tabaci a slow increase phase and a fast increase phase. (Gennadius), triazophos resistance in Chilo suppressalis Because the first 20 generations received low selection (Walker) and pyrethroid resistance in Helicoverpa pressure (non-continuous selection), the resistance armigera (Hubner).¨ 22,29– 32 development was relatively slow. Resistance ratios Many factors might be associated with the resistance also tended to fluctuate with the short term of increase in N. lugens. In terms of outbreak frequency, termination and resumption of selection. Unlike the the planthopper is classified as an intermediate out- early generations, generations 21 to 53 received breaking pest with 2–3 population outbreaks every continuous selection of buprofezin. Subsequently, 10 years in China.33 Buprofezin was used once a year the resistance levels increased at a substantially when the population density was low, and 2–3 times faster pace than those of the early generations.

1054 Pest Manag Sci 64:1050–1056 (2008) DOI: 10.1002/ps Susceptibility of Nilaparvata lugens to buprofezin

The results also showed that the planthopper ACKNOWLEDGMENTS has the potential to achieve an extremely high The authors are grateful to Prof. Xianian Cheng level of resistance if a population receives high (Nanjing Agricultural University) for his advice, and to selection pressure, as seen in the laboratory during Dr Xinzhi Ni (USDA-ARS, Tifton, GA) and Dr Ming the continuous selection experiment. The present Shun Chen (USDA-ARS, Manhattan, KS) for their resistance selection data also suggest that, if this valuable comments and suggestions for improving laboratory phenomenon could represent a field an early version of this manuscript. This research situation, alternation and rotation of buprofezin was funded by the Replacing High-toxicity Pesticides with other classes of insecticides would certainly Program of the China Ministry of Agriculture. delay and slow down resistance development to buprofezin in N. lugens. 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